Plant defense resistance in natural enemies of a specialist insect herbivore

Autor: Chad Nielson, Christelle A. M. Robert, Carla C. M. Arce, Lingfei Hu, Bruce E. Hibbard, Sandra Gruenig, Matthias Erb, Ricardo A. R. Machado, Maxime R. Hervé, Christian Parisod, Cong van Doan, Xi Zhang
Přispěvatelé: University of Bern, ARS, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, 157884, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, USDA-ARS : Agricultural Research Service, Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Université de Rennes 1 (UR1), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Jazyk: angličtina
Rok vydání: 2019
Předmět:
0106 biological sciences
0301 basic medicine
Biocontrôle
Biological pest control
biological control
Insect
580 Plants (Botany)
natural enemies
Western corn rootworm
01 natural sciences
Predation
Rhabditida
coevolutionary arms race
plant secondary metabolism
plant–herbivore interactions
tritrophic interactions
Plant defense against herbivory
Plant secondary metabolism
media_common
2. Zero hunger
chrysomele du mais
Multidisciplinary
Ecology
biology
food and beverages
Biological Sciences
Coleoptera
ennemi naturel
nématode entomopathogène
insect nematodes
Food Chain
media_common.quotation_subject
metabolite
herbivore
Zea mays
Host-Parasite Interactions
03 medical and health sciences
Evolutionary arms race
Animals
Herbivory
défense de la plante
Herbivore
fungi
15. Life on land
biology.organism_classification
Benzoxazines
[SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology
030104 developmental biology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
contrôle biologique
010606 plant biology & botany
[SDV.EE.IEO]Life Sciences [q-bio]/Ecology
environment/Symbiosis
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Proceedings of the National Academy of Sciences of the United States of America, National Academy of Sciences, 2019, 116 (46), pp.23174-23181. ⟨10.1073/pnas.1912599116⟩
Proceedings of the National Academy of Sciences of the United States of America, 2019, 116 (46), pp.23174-23181. ⟨10.1073/pnas.1912599116⟩
Zhang, Xi; van Doan, Cong; Arce, Carla C. M.; Hu, Lingfei; Gruenig, Sandra; Parisod, Christian; Hibbard, Bruce E.; Hervé, Maxime R.; Nielson, Chad; Robert, Christelle A. M.; Machado, Ricardo A. R.; Erb, Matthias (2019). Plant defense resistance in natural enemies of a specialist insect herbivore. Proceedings of the National Academy of Sciences of the United States of America-PNAS, 116(46), pp. 23174-23181. National Academy of Sciences NAS 10.1073/pnas.1912599116
ISSN: 0027-8424
1091-6490
DOI: 10.1073/pnas.1912599116⟩
Popis: Significance Certain adapted insect herbivores utilize plant toxins for self-defense against their own enemies. These adaptations structure ecosystems and limit our capacity to use biological control agents to manage specialized agricultural pests. We show that entomopathogenic nematodes that are exposed to the western corn rootworm, an important agricultural pest that sequesters defense metabolites from maize, can evolve resistance to these defenses. Resisting the plant defense metabolites likely allows the nematodes to infect and kill the western corn rootworm more efficiently. These findings illustrate how predators can counter the plant-based resistance strategies of specialized insect herbivores. Breeding or engineering biological control agents that resist plant defense metabolites may improve their capacity to kill important agricultural pests such as the western corn rootworm.
Plants defend themselves against herbivores through the production of toxic and deterrent metabolites. Adapted herbivores can tolerate and sometimes sequester these metabolites, allowing them to feed on defended plants and become toxic to their own enemies. Can herbivore natural enemies overcome sequestered plant defense metabolites to prey on adapted herbivores? To address this question, we studied how entomopathogenic nematodes cope with benzoxazinoid defense metabolites that are produced by grasses and sequestered by a specialist maize herbivore, the western corn rootworm. We find that nematodes from US maize fields in regions in which the western corn rootworm was present over the last 50 y are behaviorally and metabolically resistant to sequestered benzoxazinoids and more infective toward the western corn rootworm than nematodes from other parts of the world. Exposure of a benzoxazinoid-susceptible nematode strain to the western corn rootworm for 5 generations results in higher behavioral and metabolic resistance and benzoxazinoid-dependent infectivity toward the western corn rootworm. Thus, herbivores that are exposed to a plant defense sequestering herbivore can evolve both behavioral and metabolic resistance to plant defense metabolites, and these traits are associated with higher infectivity toward a defense sequestering herbivore. We conclude that plant defense metabolites that are transferred through adapted herbivores may result in the evolution of resistance in herbivore natural enemies. Our study also identifies plant defense resistance as a potential target for the improvement of biological control agents.
Databáze: OpenAIRE